Herbaria as critical resources for studying plant-virus biodiversity and epidemiology

IF 2.7 2区 生物学 Q2 PLANT SCIENCES
Elizabeth M. Lombardi, Hannah E. Marx
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While not all viruses are pathogenic (Roossinck, <span>2011</span>; Takahashi et al., <span>2019</span>), crop diseases caused by viral symbionts undermine food and economic security worldwide (Bos, <span>1982</span>; Sastry and Zitter, <span>2014</span>; Trębicki and Finlay, <span>2018</span>; Rao and Reddy, <span>2020</span>), and the consequences of viruses on plant biodiversity and ecosystems are understudied (Kamitani et al., <span>2016</span>; Jones and Naidu, <span>2019</span>; Lefeuvre et al., <span>2019</span>). Better data regarding spatiotemporal patterns in plant-virus distributions is a prerequisite for understanding how viruses move, change, and emerge as threats to food and ecosystem security.</p><p>One way that temporal trends in virus biodiversity may be studied is through use of natural history collections (Cook et al., <span>2020</span>; Thompson et al., <span>2021</span>), which offer the opportunity to retrospectively characterize host–virus interactions, thus building a baseline to which contemporary analyses may be compared. Similarly, Cook et al. (<span>2020</span>) demonstrate the potential benefit of using historical host specimens to efficiently survey for virus diversity across taxa and environments. This work, like most specimen-based research into historical virus diversity, focused on animal hosts. Here we discuss opportunities that would arise from utilizing plant collections in a similar fashion; while the practical and technical details of isolating plant-associated viruses from historical tissue differ from methods for other taxonomic groups, the benefits to research and disease management would be similar and numerous.</p><p>There are multiple possible virus isolate types that may be useful in studying historical plant virus communities, including agricultural isolates and “forgotten” frozen tissue specimens collected by academic and agricultural researchers (Jones et al., <span>2021</span>). We discuss pros and cons of using different tissue sources and conclude that usefulness of whole-host data from herbarium specimens justifies investment in development and research. Our objectives in this commentary are to (1) review and compare current resources and approaches available for studying plant-associated virus diversity in the context of natural history and (2) outline steps to improve global plant-virus biodiversity monitoring and preservation going forward.</p><p>Plant viruses are ubiquitous across host taxa and environments, but little is known regarding the history and biogeography of plant–virus interactions in wild plant communities. Herbaria are rich and opportune whole-host resources that may provide insight into fundamental questions about the mechanisms and consequences of plant–virus symbioses for theoretical and practical use. At this time, the principal requirement to make use of these vast biodiversity collections is the development of adequate methods to determine how feasible and biased reassembled virus communities are when isolated from pressed botanical specimens. Additionally, we advocate for new collections of atypical-looking plants and encourage subsampling of whole-plant specimens to preserve tissue in cryostorage or in silica. Finally, collaborative and transdisciplinary research teams working out of herbaria can provide important insight for the biosecurity of plant communities and crops across the planet, with opportunities to improve equitable coverage of data and resources going forward. Because viruses are global, so too are their hosts and humans who may study them; we anticipate an exciting, integrative future uncovering this universally understudied axis of plant biodiversity.</p><p>E.M.L. contributed to conceptualization, data acquisition and analyses, visual aid creation, manuscript writing, revision and editing. 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引用次数: 0

Abstract

In the wake of a virus-mediated global health crises, research has rightfully focused on monitoring zoonotic viruses, particularly those that are emerging or novel in human populations (Baker et al., 2022). Viruses that infect plants are also worthy candidates for research investment and, depending on host outcomes, epidemiological action (Anderson et al., 2004; Jones and Naidu, 2019; Jones et al., 2021). While not all viruses are pathogenic (Roossinck, 2011; Takahashi et al., 2019), crop diseases caused by viral symbionts undermine food and economic security worldwide (Bos, 1982; Sastry and Zitter, 2014; Trębicki and Finlay, 2018; Rao and Reddy, 2020), and the consequences of viruses on plant biodiversity and ecosystems are understudied (Kamitani et al., 2016; Jones and Naidu, 2019; Lefeuvre et al., 2019). Better data regarding spatiotemporal patterns in plant-virus distributions is a prerequisite for understanding how viruses move, change, and emerge as threats to food and ecosystem security.

One way that temporal trends in virus biodiversity may be studied is through use of natural history collections (Cook et al., 2020; Thompson et al., 2021), which offer the opportunity to retrospectively characterize host–virus interactions, thus building a baseline to which contemporary analyses may be compared. Similarly, Cook et al. (2020) demonstrate the potential benefit of using historical host specimens to efficiently survey for virus diversity across taxa and environments. This work, like most specimen-based research into historical virus diversity, focused on animal hosts. Here we discuss opportunities that would arise from utilizing plant collections in a similar fashion; while the practical and technical details of isolating plant-associated viruses from historical tissue differ from methods for other taxonomic groups, the benefits to research and disease management would be similar and numerous.

There are multiple possible virus isolate types that may be useful in studying historical plant virus communities, including agricultural isolates and “forgotten” frozen tissue specimens collected by academic and agricultural researchers (Jones et al., 2021). We discuss pros and cons of using different tissue sources and conclude that usefulness of whole-host data from herbarium specimens justifies investment in development and research. Our objectives in this commentary are to (1) review and compare current resources and approaches available for studying plant-associated virus diversity in the context of natural history and (2) outline steps to improve global plant-virus biodiversity monitoring and preservation going forward.

Plant viruses are ubiquitous across host taxa and environments, but little is known regarding the history and biogeography of plant–virus interactions in wild plant communities. Herbaria are rich and opportune whole-host resources that may provide insight into fundamental questions about the mechanisms and consequences of plant–virus symbioses for theoretical and practical use. At this time, the principal requirement to make use of these vast biodiversity collections is the development of adequate methods to determine how feasible and biased reassembled virus communities are when isolated from pressed botanical specimens. Additionally, we advocate for new collections of atypical-looking plants and encourage subsampling of whole-plant specimens to preserve tissue in cryostorage or in silica. Finally, collaborative and transdisciplinary research teams working out of herbaria can provide important insight for the biosecurity of plant communities and crops across the planet, with opportunities to improve equitable coverage of data and resources going forward. Because viruses are global, so too are their hosts and humans who may study them; we anticipate an exciting, integrative future uncovering this universally understudied axis of plant biodiversity.

E.M.L. contributed to conceptualization, data acquisition and analyses, visual aid creation, manuscript writing, revision and editing. H.E.M. contributed to conceptualization, manuscript writing, revision, and editing.

Abstract Image

植物标本室是研究植物病毒生物多样性和流行病学的重要资源。
在病毒介导的全球卫生危机之后,研究的重点是监测人畜共患病毒,特别是那些在人群中新出现或新的病毒(Baker等人,2022年)。感染植物的病毒也值得进行研究投资,并根据宿主的结果采取流行病学行动(Anderson等人,2004;Jones and Naidu, 2019;Jones et al., 2021)。虽然并非所有病毒都具有致病性(Roossinck, 2011;Takahashi等人,2019),由病毒共生体引起的作物病害破坏了全球的粮食和经济安全(Bos, 1982;萨斯特里和齐特,2014;Trębicki and Finlay, 2018;Rao和Reddy, 2020),病毒对植物生物多样性和生态系统的影响尚未得到充分研究(Kamitani等人,2016;Jones and Naidu, 2019;Lefeuvre et al., 2019)。关于植物病毒分布时空格局的更好数据是了解病毒如何移动、变化和出现以威胁粮食和生态系统安全的先决条件。研究病毒生物多样性时间趋势的一种方法是利用自然历史藏品(Cook等人,2020年;Thompson等人,2021),这提供了回顾性表征宿主-病毒相互作用的机会,从而建立了可与当代分析进行比较的基线。同样,Cook等人(2020)证明了利用历史宿主标本有效调查不同分类群和环境中的病毒多样性的潜在好处。与大多数基于标本的历史病毒多样性研究一样,这项工作主要集中在动物宿主上。在这里,我们将讨论以类似的方式利用植物收集所产生的机会;虽然从历史组织中分离植物相关病毒的实际和技术细节与其他分类群体的方法不同,但对研究和疾病管理的好处将是相似的,而且数量众多。有多种可能的病毒分离株类型可能对研究历史上的植物病毒群落有用,包括农业分离株和学术和农业研究人员收集的“被遗忘的”冷冻组织标本(Jones et al., 2021)。我们讨论了使用不同组织来源的利弊,并得出结论,从植物标本馆标本中获得的全宿主数据的有效性证明了在开发和研究方面的投资是合理的。我们在这篇评论中的目的是:(1)回顾和比较目前在自然历史背景下研究植物相关病毒多样性的资源和方法;(2)概述未来改善全球植物相关病毒多样性监测和保护的步骤。植物病毒在宿主分类群和环境中普遍存在,但对野生植物群落中植物-病毒相互作用的历史和生物地理学知之甚少。植物标本室是丰富和适宜的全宿主资源,可以为理论和实际应用提供有关植物-病毒共生机制和后果的基本问题的见解。目前,利用这些庞大的生物多样性集合的主要要求是发展适当的方法,以确定从压制的植物标本中分离出来的重组病毒群落的可行性和偏差程度。此外,我们提倡收集新的非典型外观的植物,并鼓励整个植物标本的亚采样,以保存组织在低温储存或二氧化硅。最后,在植物标本馆工作的协作和跨学科研究团队可以为全球植物群落和作物的生物安全提供重要见解,并有机会改善数据和资源的公平覆盖。因为病毒是全球性的,所以它们的宿主和研究它们的人类也是全球性的;我们期待着一个令人兴奋的、整合的未来,揭示这个普遍未被充分研究的植物生物多样性轴。参与概念化,数据采集和分析,视觉辅助创建,手稿写作,修改和编辑。H.E.M.参与了构思、手稿撰写、修订和编辑工作。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
American Journal of Botany
American Journal of Botany 生物-植物科学
CiteScore
4.90
自引率
6.70%
发文量
171
审稿时长
3 months
期刊介绍: The American Journal of Botany (AJB), the flagship journal of the Botanical Society of America (BSA), publishes peer-reviewed, innovative, significant research of interest to a wide audience of plant scientists in all areas of plant biology (structure, function, development, diversity, genetics, evolution, systematics), all levels of organization (molecular to ecosystem), and all plant groups and allied organisms (cyanobacteria, algae, fungi, and lichens). AJB requires authors to frame their research questions and discuss their results in terms of major questions of plant biology. In general, papers that are too narrowly focused, purely descriptive, natural history, broad surveys, or that contain only preliminary data will not be considered.
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